Patients with intralesional hemorrhage in venous malformations: Diagnosis and embolosclerotherapy
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1 Patients with intralesional hemorrhage in venous malformations: Diagnosis and embolosclerotherapy Hui Chen, MD, Xiaoxi Lin, MD, Yunbo Jin, MD, Wei Li, MD, Gang Ma, MD, and Xiaojie Hu, MD, Shanghai, China Purpose: Venous malformations (VMs) are common congenital benign lesions characterized by slow progression. However, intralesional hemorrhage can result in sudden enlargement of the lesions, which, though uncommon clinically, brings difficulties in diagnosis and treatment. The purpose of this study is to explore the clinical features and diagnosis modality of intralesional hemorrhage in VMs and present our experience with embolosclerotherapy. Methods: A series of 16 patients were recruited from May 2003 to February 2007, of which fifteen were males and one was female, aged from five months to 40 years (mean, 11.4 years). The anatomic sites affected included cheek (n 6), upper lid (n 3), neck (n 3), parotid region (n 2), temple (n 1), and upper limb (n 1). The period of enlargement varied from one day to 25 days (mean, 8.4 days). Diagnostic needle aspiration was performed to analyze the internal contents of the masses by macroscopic observation. Magnetic resonance imaging (MRI) was applied to determine the size, location, and extent of the lesions. Two patients received percutaneous venography. Routine blood testing was carried out in all cases. A combination of absolute alcohol and Bleomycin A5 embolosclerotherapy was administered to the patients. The procedure was repeated after 6 to 8 weeks. Outcomes were assessed by MRI measurement and pre and post treatment color photos. Results: All the patients were diagnosed with hemorrhage in VMs. The volume of the localized lesions varied from 3cm 2cm 1cmto8cm 5cm 3 cm. Fourteen patients received embolosclerotherapy in one (n 10) or two (n 4) sessions. Two cases were not treated and the lesions regressed spontaneously with detectable residual lesions. After a mean follow-up of 25 months (range, 3 to 40 months), treatment was considered effective in 12 patients. The complications were minimal including temporary swelling in 14 treated patients and mild fever in two patients. Conclusion: Intralesional hemorrhage in VMs should be distinguished from other lesions in the head and neck region. Diagnostic puncture and MRI are essential for accurate diagnosis. Percutaneous embolosclerotherapy using a combination of absolute ethanol and Bleomycin A5 is a safe and effective treatment of choice. (J Vasc Surg 2009;49: ) Venous malformations (VMs) are common congenital anomalies of vascular morphogenesis. The lesions grow commensurately with the child s development and do not show involution. 1,2 It is uncommon for the lesions to expand suddenly within a few days. However, if intralesional hemorrhage occurs, the lesions may enlarge rapidly, which is quite dissimilar to their natural history. Misdiagnosis or improper treatment may occur if attending physicians are not familiar with this situation. In the past four years, a total of 16 patients with intralesional hemorrhage in VMs were treated in our department. We performed a retrospective study of those cases and confirmed that clinical history, physical examination, diagnostic needle aspiration, and magnetic resonance imaging (MRI) findings were essential to establish a correct diagnosis. Meanwhile, percutaneous embolosclerotherapy using a combination of absolute ethanol and Bleomycin A5 has been performed in our department for the treatment of From the Shanghai Ninth People s Hospital. Competition of interest: none. Reprint requests: Dr. Xiaoxi Lin, Shanghai Ninth People s Hospital, Department of Plastic Surgery, 639# Zhizaoju Rd., Shanghai , China ( linxiaoxi@126.com) /$36.00 Copyright 2009 Published by Elsevier Inc. on behalf of The Society for Vascular Surgery. doi: /j.jvs common VMs (VMs without hemorrhage). The safety and effectiveness of this therapy has been well established. 3 Our aim was to extend the use of this method to treat patients with intralesional hemorrhage in VMs. The purpose of this study was to explore the clinical features, diagnosis, and differential diagnosis of intralesional hemorrhage in VMs and develop an effective treatment method. PATIENTS AND METHODS Patients. From May 2003 to February 2007, 16 patients with intralesional hemorrhage in VMs were included in this study. Those included 15 males and 1 female aged from 5 months to 40 years (mean, 11.4 years). The anatomic sites affected included cheek (n 6), upper lid (n 3), neck (n 3), parotid region (n 2), temple (n 1), and upper limb (n 1). The period of enlargement varied from 1 day to 25 days (mean, 8.4 days). Six patients provided specific trauma histories (blunt trauma in three cases and intensive joint movements in the other three cases). Three patients complained of pre-existing masses before the onset of hemorrhage. At their first visit to the department, diagnostic needle aspiration was performed in all patients to analyze the internal contents of the masses by macroscopic observation. MRI was applied in defining the size, location, and extent 429
2 430 Chen et al JOURNAL OF VASCULAR SURGERY February 2009 Fig 1. a, A 14-year-old boy with a lesion in the left cheek. b, Two years after one treatment. c, A small residual lesion was revealed in MRI (arrow). d, Normal venous blood was aspirated from the residual lesion that was supportive for the diagnosis of intralesional hemorrhage in venous malformations. of the lesions. Two patients received percutaneous venography. Routine blood testing was carried out in all cases. Treatment techniques. Written informed consent was obtained from the patients or their parents before treatment. The first procedure began when the lesions stopped expanding and were stabilized for one week. Six pediatric patients were treated under general anesthesia and the other patients without anesthesia. After preparation of the treatment site with povidoneiodine, 1-2 ml blood was aspirated out of the lesion by a 5 ml-syringe to check for blood again. Then a direct puncture was performed using 21-gauge needles. At each session, 2-6 injection sites were needed according to the size of the lesions. Once the blood returned, 1-3 ml absolute alcohol was injected first, followed by a maximum of 8 mg of bleomycin A5 after 1 to 2 minutes (8 mg dissolved in 4 ml 0.9% sodium chloride). The maximum dose in a single procedure was 0.1 ml/kg for absolute alcohol and 0.2 mg/kg for Bleomycin A5. The treatment was repeated if there was detectable residual mass and confirmed by a direct puncture (venous blood return). The interval between two procedures was 6-8 weeks. Outcome evaluation. MRI and pre- and post-treatment color photos were applied in outcome evaluation. Due to the limited number of cases, we used two categories for outcome evaluation. The treatment was considered effective if the volume of the lesion was reduced 75% (measured by MRI parameters) or significant improvements in appearance were observed and the patient requested no further treatment. The treatment was considered ineffective if the volume of the lesion was reduced 75% or the patient was not satisfied with the improvements in appearance. RESULTS All the patients were diagnosed with intralesional hemorrhage in VMs (Fig 1). No abnormal hematologic findings were observed in routine blood testing. Fifteen patients developed localized lesions and 1 patient had an infiltrating lesion. The volume of the localized lesions varied from 3 cm 2cm 1cmto8cm 5cm 3 cm measured by MRI. The infiltrating lesion was not measured. Fourteen patients received embolosclerotherapy with one (n 10) or two (n 4) procedures. At a mean follow-up of 25 months (range, 3-40 months), treatment was considered effective in 12 patients. Percentage of volume reduction was 82% to 100% (mean, 93%).The patients recovered to nearly normal appearance and asked for no further treatment. Three cases manifested complete resolution of the lesions (Fig 2). In two infantile cases with lesions involving upper eyelids, the treatment was ineffective due to unsatisfactory appearance improvements with a clearance rate of 50% and their parents declined further treatment. Patients follow-up showed stable lesions. The two patients who were not treated were monitored for 4 years and 4 months respectively. The lesions resolved spontaneously after 2 months, but the residual lesions exhibited typical VM features, which corroborated our initial diagnosis (Fig 3). The complications were generally minimal. All treated patients experienced a degree of local swelling that regressed without any therapy after 5 to 10 days. Two patients complained of mild fever that disappeared after 2 days. No major or permanent complications occurred. There was no clinical or MRI evidence of recurrence in the treated cases. DISCUSSION Pathogenesis of intralesional hemorrhage in VMs. Even though the pathogenesis of intralesional hemorrhage in VMs is not well recognized, it may have a close relationship with the abnormal structure of the vascular wall. The VMs are formed by thin-walled channels, deficient in smooth muscle cells and lined by a single layer of endothelium. 4 There are slit-like or interconnected channels dissecting through normal tissues. These veins will dilate over time because of repeated engorgement. 5
3 JOURNAL OF VASCULAR SURGERY Volume 49, Number 2 Chen et al 431 Fig 2. A 3-year-old boy with a lesion in the left cheek. The evident bruise on his left cheek was a sign of subcutaneous hemorrhage. He had no trauma history. a, Before treatment. b, Five months after one session. c, Magnetic resonance imaging revealed a well-defined margin of inhomogenous high-singal intensity area in the left cheek. d, The lesion resolved completely 5 months later. Not all patients have noticeable VMs at birth because in early anomalous veins the blood flow is slow with stable hemodynamics. During puberty or pregnancy, the lesions tend to grow more rapidly, which is stimulated by hormonal effects. However, such sudden enlargement as we have described in this study may not happen during puberty or pregnancy. Trauma is considered to be one of the important factors contributing to sudden growth of the lesions. Intensive movements of the joints have the same effects as blunt trauma, such as temporomandibular joint, shoulder joint, or elbow joint. The clear history of intensive joint movements in our three cases proved this. The blood escapes out of the ruptured veins and accumulates in the adjacent venous sinuses. Not all the VMs have sufficient peripheral drainage according to their anatomy and hemodynamic features. 6 Such blood flow disturbances may change the stable hemodynamics and peripheral drainage of the VMs so that more veins are perfused and dilated rapidly in a short time. The duration of enlargement varied from one to 25 days in our study. If not treated, the expanded lesions would regress gradually, but residual lesions were noticeable. In this study, only 6 patients provided clear trauma histories; the bleeding etiology of the other cases was unknown. The normal routine blood testing excluded hematologic disease that may cause bleeding on the whole. Diagnosis and differential diagnosis. Final diagnosis of the intralesional hemorrhage in venous malformations relied on the combination of the clinical history, clinical presentation, diagnostic needle aspiration, and MRI findings. Clinical history is important to the diagnosis for a sudden enlarged mass. The following three types of signs could be more supportive: clear history of direct blunt
4 432 Chen et al JOURNAL OF VASCULAR SURGERY February 2009 Fig 3. a, A 16-year-old boy had an extensive mass involving his left neck. The mass enlarged abruptly overnight after intense exercises. He was not treated. b, Four months later, the mass had regressed and previous lesion still existed. Small and hard nodules could be felt under the skin (arrow). c, Magnetic resonance imaging revealed numerous phleboliths within the lesion (arrow). trauma to the lesion; pre-existing mass; and self-regressed lesions proven to be VM by long-term follow-up. On physical examination, the lesion presented a localized, prominent, and tense mass at palpation under normal or purple skin. The purple skin was an obvious symptom of subcutaneous hemorrhage. No pulsate or thrill could be detected. Diagnostic needle aspiration was useful to identify whether the lesion was formed by vascular channels. Even without the negative pressure aspiration by a syringe, the blood could flow out from the end of the needle easily. By macroscopic observation, except for being slightly darker in color, the blood had the same characteristics as normal venous blood without any suspicious components. These findings do not occur in solid or cystic tumors. MRI plays a leading role in the diagnosis of different type of vascular anomalies. MRI is powerful in its ability to delineate the extent of the lesions and the relationship to the adjacent tissues and organs, 7,8 which was the most important imaging modality to guide our treatment. In the case of an infiltrating lesion, phleboliths were revealed by MRI that made the diagnosis more convincing. However, it is difficult to distinguish the bleeding VMs from common VMs (VMs without intralesional bleeding), especially large lesions, by MRI. However, MRI can be used to exclude other type of tumors. The most confusing lesions are intralesional bleeding in lymphangiomas. MRI showed a tumor with sharp border, homogenous intensity, a fluid-fluid level, and no signal enhancement. By needle aspiration, the blood is brown to black, viscous but not clotting. In two patients, we performed percutaneous direct puncture phlebography to see whether the bleeding was in VMs or in lymphangiomas. The lesion was proved to be VM due to the emergence of draining veins. Phlebography is used as a road map to guide the treatment of the VMs with high risk, while rarely needed for the differential diagnosis. Other tumors in the head and neck region with similar presentations to bleeding VMs include false aneurysm, branchial cleft cyst, and parotid cyst. False aneurysms may arise following traumatic damage to an artery and are comprised of a slowly expanding blood-filled cavity, which is held around the artery by connective tissue. But generally it is a mass with pulsate and thrill, which is similar to arteriovenous malformations (AVMs) but not to VMs. Branchial cleft cysts and parotid cysts can be distinguished by the findings of cholesterol crystal and positive amylase test for aspirated liquid. Evaluation of combination embolosclerotherapy. In recent years, absolute alcohol has been the most commonly used liquid agent for the percutaneous embolization of VMs. 9 As absolute alcohol can result in severe endothelial denudation and thrombosis immediately, it is the only known and clinically tested effective scleroagent to be able to abrogate endothelial cells, with the prospect of a cure in selected cases A response rate of 74% to 91% with limited to no recurrence has been reported. 10,11,13,14 Bleomycin A5 is a refined ingredient from Bleomycin with more potent antitumor abilities. Bleomycin can produce a sclerosing effect on the endothelial cells of the vessels. Minor complications were reported in the treatment of VMs. 15 Since 2002, we have used the two sclerosing agents in combination in our department. This combination therapy has been proven to be very effective with only minor complications when treating common VMs. 3 Here we have reported that this method was also a treatment of choice for VMs with intralesional bleeding. Most of the bleeding lesions were limited with predictable favorable outcomes. However, because the bleeding lesions were different from non-bleeding ones after all, we could not tell if our method
5 JOURNAL OF VASCULAR SURGERY Volume 49, Number 2 Lee 433 was superior to treatment with single sclerosing agents and further study is warranted. CONCLUSION Intralesional hemorrhage in VMs is uncommon. Accurate diagnosis and differential diagnosis should be based on the history, clinical presentations, diagnositic needle aspiration, and MRI findings. Percutaneous absolute ethanol and Bleomycin A5 embolosclerotherapy is a safe and effective treatment of choice. We would like to thank Nagalakshmi Nadiminty, PhD, (Assistant Professor, Department of Urology and Cancer Center, University of California Davis Medical Center, Sacramento, Calif), Elaine Pinder, PhD, candidate (Graduate Program of Pharmacology and Toxicology, University of California Davis, Davis, Calif), and Siting Feng, MD, PhD, candidate, (Department of Cardiology, Renmin Hospital, Wuhan University, Wuhan, China) for their assistance in the preparation of this manuscript. AUTHOR CONTRIBUTIONS Conception and design: XL Analysis and interpretation: XL, HC Data collection: XL, HC, YJ, WL, GM, XH Writing the article: HC Critical revision of the article: XL, HC, YJ Final approval of the article: XL Statistical analysis: Not applicable Obtained funding: Not applicable Overall responsibility: XL REFERENCES 1. Enjolras O, Mulliken JB. Vascular tumors and vascular malformations (new issues). Adv Dermatol 1997;13: Mulliken JB, Glowacki J. Hemangiomas and vascular malformations in infants and children: a classification based on endothelial characteristics. Plast Reconstr Surg 1982;69: Jin Y, Lin X, Li W, Hu X, Ma G, Wang W. Sclerotherapy after embolization of draining vein: a safe treatment method for venous malformations. J Vasc Surg 2008;47: Claudon M, Upton J, Burrows PE. Diffuse venous malformations of the upper limb: morphologic characterization by MRI and venography. Pediatr Radiol 2001;31: Hein KD, Mulliken JB, Kozakewich HPW, Upton J, Burrows PE. Venous malformations of skeletal muscle. Plast and Reconstr Surg 2002;110: Puig S, Aref H, Chigot V, Bonin B, Brunelle F. Classification of venous malformations in children and implications for sclerotherapy. Pediatr Radiol 2003;33: Fayad LM, Hazirolan T, Bluemke D, Mitchell S. Vascular malformations in the extremities: emphasis on MR imaging features that guide treatment options. Skeletal Radiol 2006;35: Lee BB, Mattassi R, Loose D, Yakes W, Tasnadi G, Kim HH. Consensus on controversial issues in contemporary diagnosis and management of congenital vascular malformation: Seoul communication. Int J Angiol 2005;13: Puig S, Casati B, Staudenherz A, Paya K. Vascular low-flow malformations in children: current concepts for classification, diagnosis and therapy. Eur J Radiol 2005;53: Lee BB, Kim DI, Huh S, Kim HH, Choo IW, Byun HS, et al. New experiences with absolute ethanol sclerotherapy in the management of a complex form of congenital venous malformation. J Vasc Surg 2001; 33: Lee BB, Do YS, Byun HS, Choo IW, Kim DI, Huh SH. Advanced management of venous malformation with ethanol sclerotherapy: midterm results. J Vasc Surg 2003;37: Yakes WF, Haas DK, Parker SH, Gibson MD, Hopper KD, Mulligan JS, et al. Symptomatic vascular malformations: ethanol embolotherapy. Radiology 1989;170: Goyal M, Causer PA, Armstrong D. Venous vascular malformations in pediatric patients: comparison of results of alcohol sclerotherapy with proposed MR imaging classification. Radiology 2002;223: Mason KP, Michna E, Zurakowski D, Koka BV, Burrows PE. Serum ethanol levels in children and adults after ethanol embolization or sclerotherapy for vascular anomalies. Radiology 2000;217: Zhi K, Wen Y, Li L, Ren W. The role of intralesional Pingyangmycin in the treatment of venous malformation of facial and maxillary region. Int J Pediatr Otorhinolaryngol 2008;72: Submitted May 27, 2008; accepted Aug 20, INVITED COMMENTARY Byung-Boong Lee, MD, Reston, Va In this article, the authors describe the successful management of 16 patients with relatively sudden enlargement of a venous malformation (VM) due to acute hemorrhage. This represents a small subset of patients with VMs since the majority of VMs do not develop intra-lesion hemorrhage. The authors report good results using a combination of ethanol and bleomycin as the sclerosing agent. While the use of the powerful sclerosing agent absolute ethanol is quite well accepted for treating more aggressive arteriovenous malformations, its use in VM is more limited. This is because of serious potential complications reported with its use, including acute complications of nerve palsy or even cardiopulmonary arrest. 1,2 Therefore, many have begun to consider the use of less dangerous sclerosing agents, such as detergent-based foam, especially for less aggressive VMs, including those with transdermal extension in which there is a higher risk for complications from ethanol injection. Although foam sclerotherapy is likely less effective than ethanol, the complication rate is lower, and if VMs recur, or are only partially treated initially, they can be re-treated with foam sclerotherapy with fewer overall complications. The authors attempted to reduce the risk involved with ethanol injection of the VM by mixing it with bleomycin. However, it is difficult to judge the contribution of bleomycin to the overall treatment outcome since the ethanol was given first to block the draining veins; regardless of its amount, there is substantial risk of the vascular spasm induced by the ethanol before bleomycin begins to work, reducing its effective contact with the endothelial cells. Bleomycin was used extensively to various lymphatic malformations (LMs) with excellent result for the macrocystic lesions in particular. 3,4 It still remains a major option when OK-432 (Chugai Pharmaceutical, Tokyo, Japan), also known as picibanil, which is made with attenuated streptococcal exotoxin, is not available for the LM. 5,6 However, we have found bleomycin is generally less effective when the LM is mixed with the VM. Furthermore, the potential concern for pulmonary fibrosis as a long-term complication of bleomycin remains to be answered especially when it is injected to the VM/venous system. This potential long-term concern has led us not to use bleomycin for VM treatment.
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